Horseshoe bats and Old World leaf-nosed bats have two discrete types of pinna motions Xiaoyan YinPeiwen QiuLili YangRolf Müller Citation: The Journal of the Acoustical Society of America 141, 3011 (2017); doi: 10.1121/1.4982042 View online: http://dx.doi.org/10.1121/1.4982042 View Table of Contents: http://asa.scitation.org/toc/jas/141/5 Published by the Acoustical Society of America Articles you may be interested in Measurement of low-frequency tissue response of the seagrass Posidonia oceanica The Journal of the Acoustical Society of America 141, (2017); 10.1121/1.4981925 Three-dimensional sonar beam-width expansion by Japanese house bats (Pipistrellus abramus) during natural foraging The Journal of the Acoustical Society of America 141, (2017); 10.1121/1.4981934 Horseshoe bats and Old World leaf-nosed bats have two discrete types of pinna motions Xiaoyan Yin Shandong University–Virginia Tech International Laboratory, 27 Shanda South Road, Jinan, Shandong 250100, People’s Republic of China Peiwen Qiu Department of Mechanical Engineering, 1075 Life Science Circle, Virginia Tech, Blacksburg, Virginia 24061, USA Lili Yang Shandong University–Virginia Tech International Laboratory, 27 Shanda South Road, Jinan, Shandong 250100, People’s Republic of China Rolf Muller€ a) Department of Mechanical Engineering, 1075 Life Science Circle, Virginia Tech, Blacksburg, Virginia 24061, USA (Received 5 December 2016; revised 3 March 2017; accepted 10 April 2017; published online 2 May 2017) Horseshoe bats (Rhinolophidae) and the related Old World leaf-nosed bats (Hipposideridae) both show conspicuous pinna motions as part of their biosonar behaviors. In the current work, the kine- matics of these motions in one species from each family (Rhinolophus ferrumequinum and Hipposideros armiger) has been analyzed quantitatively using three-dimensional tracking of land- marks placed on the pinna. The pinna motions that were observed in both species fell into two cate- gories: In “rigid rotations” motions the geometry of the pinna was preserved and only its orientation in space was altered. In “open–close motions” the geometry of the pinna was changed which was evident in a change of the distances between the landmark points. A linear discriminant analysis showed that motions from both categories could be separated without any overlap in the analyzed data set. Hence, bats from both species have two separate types of pinna motions with apparently no transitions between them. The deformations associated with open–close pinna motions in Hipposideros armiger were found to be substantially larger compared to the wavelength associated with the largest pulse energy than in Rhinolophus ferrumequinum (137% vs 99%). The role of the two different motions in the biosonar behaviors of the animals remains to be determined. VC 2017 Acoustical Society of America.[http://dx.doi.org/10.1121/1.4982042] [AMS] Pages: 3011–3017 I. INTRODUCTION in the biosonar systems of rhinolophid and hipposiderid bats goes beyond this well-known control mechanism and Horseshoe bats (rhinolophids, Rhinolophidae) and Old extends to the interfaces of ultrasound emission and recep- World leaf-nosed bats (hipposiderids, Hipposideridae) are tion. Species in both bat families emit their biosonar pulses two closely related bat families1 noted for their highly capa- nasally. It has been shown that the noseleaves, baffle shapes ble biosonar systems that allow these animals to navigate that surround the nostrils in species of both groups, can and hunt in acoustically difficult, cluttered environments change their geometry while diffracting the outgoing such as dense vegetation.2,3 One aspect that makes the bioso- pulses.8,9 Changes similar to what has been observed in the nar systems of rhinolophids and hipposiderids unique is a bats have been predicted to have an impact on the ultrasonic pervasive dynamics.4 For example, bats of both families emission characteristics by numerical simulations9,10 as well have been shown to dynamically control the carrier fre- as through experiments with biomimetic prototypes.11 quency of their sonar pulses to compensate for Doppler Furthermore, horseshoe bats have been shown to change the shifts due to their own flight motion.2,5,6 This dynamic con- widths of their biosonar beams,12 but the underlying mecha- trol enables the detection of Doppler shifts induced by the nism remains to be determined. wing motion of an insect prey and hence allows the bats to Similarly, it has been known for more than 50 years that distinguish the insect targets from vegetation clutter as well rhinolophids as well as hipposiderids have highly differenti- as classifying different insect prey.7 However, the dynamics ated ear muscles13,14 and can carry out ear motions during biosonar behaviors.15–17 First attempts at understanding the potential function of the pinna motions in rhinolophids and a)Also at: Shandong University–Virginia Tech International Laboratory, 27 Shanda South Road, Jinan, Shandong 250100, People’s Republic of China. hipposiderids have focused on representing the motion as Electronic mail: [email protected] rigid rotations that change the orientation of a time-invariant J. Acoust. Soc. Am. 141 (5), May 2017 0001-4966/2017/141(5)/3011/7/$30.00 VC 2017 Acoustical Society of America 3011 device characteristic (beampattern).18 By scanning a time- ferrumequinum,23 pinna length 2.2 cm,24 Fig. 1(b) and eight invariant sonar beam across a target, the bat would be able to were great Himalayan leaf-nosed bats [Hipposideros armi- determine the direction of a target. Such a mechanism could ger,25 seven males and one female, pinna length 3.3 cm,24 explain the experimental finding that horseshoe bats that had Fig. 1(a)]. The rhinolophids were obtained from a cave near their pinna motions disabled performed less well when Jinan, Shandong province and the hipposiderids from caves in avoiding obstacles spaced in elevation.19 However, it has two regions in southern China, in the vicinity of Sanming been demonstrated that the pinna motions in horseshoe bats city, Fujian province, and Suiyang city, Guizhou province. can be non-rigid and result in noticeable changes to the The bats were housed in indoor flight rooms (separated by geometry of the pinna.20 The magnitude of the non-rigid genus) that provided a controlled environment with constant shape changes has been shown to be similar to the ultrasonic temperature (23 C) and humidity (60%). The bats were fed a wavelengths.20 Furthermore, experiments with physical real- diet of mealworms and were provided bottled water ad izations of biomimetic deforming microphone baffles have libitum. demonstrated that non-rigid motions of similar magnitude Quantitative characterizations of the pinna motions and geometry can result in time-variant receiver were obtained based on three-dimensional reconstructions of characteristics.21,22 the positions of discrete landmark points (Fig. 1). The land- At the time of writing, the authors are aware of only a mark points were placed on the bats using a green, nontoxic single published data set on the non-rigid pinna motions in dye before the experiments and removed immediately after rhinolophids20 and no published data on the non-rigid pinna the end of each experiment. For each experiment, approxi- motions in hipposiderids appear to be available. It remains mately 60 distinct landmark points were distributed over the unclear whether all rhinolophid/hipposiderid bat pinna pinna surface with an emphasis on coverage of the pinna motions have a substantial non-rigid component or whether rim. Five to seven additional landmark points each were mostly rigid motions are also part of the animals’ repertoire. placed on the top of the head and the noseleaf of each animal Hence, the goal of the present work has been to investigate to provide an anatomical frame of reference for the pinna quantitatively which part of the range spanned by entirely motions. During the experiments, the bat was placed on a rigid and strongly non-rigid motions is occupied by the pin- platform consisting of a piece of planar wire-mesh grid that nae motions of rhinolophid and hipposiderid bats. If motions was sloping downwards with a 45 angle relative to the hori- from near both ends of this spectrum can be found, are rigid zontal. On this platform, the bat was positioned in the center and non-rigid pinna motion patterns discrete categories or of the setup (Fig. 2) and at a distance of about 50 cm from extremes of a continuum? Finally, do pinna motions in rhi- the high-speed video cameras that were used to record the nolophid and hipposiderid bats follow the same patterns or pinna motions. are there differences between these two families? To answer While the bat was on the platform, it was attempted to these questions, three-dimensional motion trajectories for a attract the animal’s attention with a rotating propeller (diam- dense set of landmarks placed on the pinnae of rhinolophid eter 9 cm, variable rotation speeds between 10 and 80 revo- and hipposiderid bats have been obtained using a high-speed lutions per second) that was designed to mimic the wing stereo vision approach. The resulting landmark data have been analyzed quantitatively yielding a metric that was used to characterize pinna motions as rigid or non-rigid. II. METHODS Pinna motion patterns were observed qualitatively or quantitatively in a study group that comprised a total of 15 individual bats. These animals belonged to two different spe- cies: seven greater horseshoe bats (Rhinolophus FIG. 2. Experimental setup: The three-dimensional motion trajectories of the landmarks on the pinnae were determined with an array of four high- speed video cameras. The echo returns were registered with a horizontal and a vertical microphone array. All cameras and microphones were triggered FIG. 1. Individuals from the two bat species for which the pinna motions simultaneously.